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Behavior and Habitat Selection of Deep-Sea Fishes

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Behavior and Habitat Selection of Deep-Sea Fishes Behavior and habitat selection of deep-sea fishes: a methodological Franz Uiblein perspective Franz Uiblein1, Fernando Bordes2, Pascal Lorance3, Jørgen G. Nielsen4, David Shale5, Marsh J. Youngbluth6 & Rupert Wienerroither7,1 1 Institute of Marine Research, P.O. Box 1870 Nordnes, N-5817 Bergen, Norway (Contact e-mail: [email protected]) 2 Instituto Canario de Ciencias Marinas, P.O.Box 56, 35200 Telde, Gran Canaria, Spain 3 IFREMER, Déartement Ecologie et Modèes pour l'Halieutique rue de l'îe d'Yeu, B.P. 21105, 44311 Nantes Cedex 03, France 4 Zoological Museum, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100, Copenhagen Ø, Denmark. 5 Flat 12, Beachside Court, 14 Victoria Avenue, Swanage, Dorset, UK 6 Harbor Branch Oceanographic Institution, 5600 US 1 North, Fort Pierce, FL 34946, USA 7 Department of Organismic Biology, Ecology and Biodiversity Research Unit, Hellbrunnerstrasse 34, A-5020 Salzburg, Austria Abstract The behavior and habitat selection of deep-sea fishes has been studied with various methods. Five of the most promising approaches to investigate the behavioral ecology are reviewed: (1) functional morphology, (2) field sampling, (3) acoustic tracking, (4) in-situ surveillance, and (5) ex-situ experimentation. Functional morphology, often a “by-product” of taxonomic and systematic studies, is strongly comparative and correlative, and serves to examine hypotheses on behavioral strategies. Field sampling with towed gear identifies vertical and horizontal distribution in the water column and deployments of stationary gear document aggregation and diversity patterns on or close to the seafloor. With acoustic instruments vertical migrations and segregation patterns can be tracked. In-situ observations with cameras and attraction devices or from underwater vehicles focus studies on behavior and habitat selection over small to large-scale intervals and distances, both vertically and horizontally. Ex-situ behavioral studies of deep-sea fishes brought to the surface have been conducted to a limited extent, mainly in unpressurized aquaria. An integrated approach which combines various methods would provide a more complete understanding of behavioral diversity and adaptations to environmental factors. Introduction The deep sea, i.e. the vast area of the oceans below 200 m water depth, is largely unexplored and basic questions related to the evolution of deep-sea organisms are unresolved, e.g., how many species live there and what are their behavioral habits? Although fishes are among the best studied fauna at greater depth, their systematics, ecology, and evolution still requires intensified research. 05 About 2700 deep-sea fish species have been described. Koslow et al. (1997) estimated that at least another 1000 species exist. Some taxa can be regarded as “ancient” deep-sea dwellers, e.g., those species that possess light organs like anglerfishes (Ceratoidei) or lanternfishes (Myctophidae). Other fishes are morphologically less differentiated and more closely related to shallow-water species (= secondary deep-sea fishes; Andriashev, 1953). Ecologically, deep-sea fishes have been grouped into open-water, Franz Uiblein pelagic, and bottom-associated, demersal species. Further depth-related subdivision considers also light penetration (to ca. 1000 m maximally) and bottom topography: mesopelagic (200 -1000 m), bathypelagic (1000 to ca. 3500 m), and abyssopelagic (>3500 m) species in the open water, bathyal (200 to ca. 3500 m; upper, mid- and lower slope) and abyssal (> 3500 m) species on the bottom. The greatest depth from which a fish has been collected is 8370 m (Nielsen, 1977). In recent years novel technologies have provided more frequent access and more detailed records in the light-reduced and hyperbaric regime of the deep sea, making it possible to answer fundamental questions about adaptations to extreme conditions. An amazing array of sampling, analyzing, and exploratory methods can now be used to study deep-sea fish behavior. We provide here an overview of the five most significant approaches: (1) functional morphology, (2) field sampling, (3) acoustic tracking, (4) in-situ surveillance, and (5) ex-situ experimentation. As we hope, this review will stimulate more research in this field. (1) Functional morphology Functional morphology arises often as a “by-product” of taxonomic and systematic studies. The approach is strongly comparative and correlative emphasizing the testing of hypotheses about behavioral strategies by investigating the adaptive significance of organism structures in relation to distinct environmental features. Functional morphological studies of deep-sea fishes have commonly focused on non-visual perception and communication modalities based on the comparative examination of chemo-tactile organs on head, body, fins, or barbels, and the structure of sound-producing organs (e.g., in grenadiers, Macrouridae, and cuskeels, Ophidiidae; see Marshall, 1979; Carter and Musick 1985; Merrett and Haedrich, 1997). Chemo-tactile sensing facilitates detection of food, predators, or conspecifics in the immediate surroundings or allows predators to track prey via currents (e.g., Wilson and Smith, 1984; Baird & Jumper, 1995). Many deep-sea fishes have large otoliths (calcium carbonate structures in the inner ear) that may have a selective sound-perception function (Paxton, 2000). Differences in otolith form among closely related species strongly suggest that they permit intraspecific communication. For instance, the two sister species of the genus Spectrunculus (Ophidiidae), S. crassus and S. grandis, co-occur in the northern Atlantic at bathyal and abyssal depths (Uiblein et al., 2008). Recent morphological comparisons leading to the resurrection of S. crassus as a valid species have shown that they clearly differ in otolith shape (Uiblein et al., 2008). Members of this family have the capability to produce sounds based on “drumming” muscles 06 that connect the swimbladder with modified ribs and the otic capsule (Merrett and Headrich, 1997). Species differences in hearing capacity and selectivity may relate to the production of species-specific sound signals Franz Uiblein and social communication in deep-sea fishes much like has been observed in shallow water species (e.g., Mann et al., 1997; Cruz and Lombarte, 2004; Rountree et al., 2006). Fig. 1. Among 50 species of the cuskeel genus Neobythites, family Ophidiidae, 39 (= 78 %) show coloration patterns. For each of the four different coloration types one species is shown as an example. The number of species showing the respective color pattern and percentages referring to the total number of colored species is also provided (after Uiblein and Nielsen, 2005). The shallowest part of the deep sea is still weakly illuminated by downwelling light. Well-developed eyes should be able to perceive sunlight until a depth of around 1000 m and distinction of contrasting colors should be possible to ca. 500-600 m depending on water clarity (Clark and Denton 1961). The latter prediction has been supported by investigations of eyespot (=ocellus) development and ontogenetic niche shifts in the ophidiid Neobythites stefanovi (Uiblein et al., 1994; Uiblein and Nielsen, 2005). This species shows typical circular to elliptical dark spots surrounded by a contrasting pale ring on the dorsal fin (Nielsen and Uiblein 1993; Fig. 1). Various functions have been ascribed to ocelli. They may reduce predation risk by, for instance, deterring visually hunting predators or deflecting their attacks to less vital parts of the body. Alternatively, they may enhance social communication and species recognition or they may serve several functions simultaneously (Uiblein and Nielsen, 2005). Neobythites stefanovi occurs on the upper slope of the Northwestern Indian Ocean and the Red Sea and has one ocellus on the dorsal fin positioned at about mid-body (Nielsen and Uiblein, 1993). In the Red Sea population, an upward-directed ontogenetic migration from about 800m to less than 600m was detected that 07 development of the ocellus (Uiblein et al., 1994; Uiblein, 1996). This observation was interpreted as an indication for ocellus antipredator function, as risk from visually hunting predators should increase in shallower and more illuminated habitats. A morphological comparison of the N. stefanovi specimens collected in the Gulf of Aden, Indian Ocean, with the generally deeper-occurring population from the adjacent Red Sea revealed a significantly higher ocellus Franz Uiblein diameter in the latter. The enlarged ocellus should intensify the signaling effect and enhance its visibility to predators at larger, less illuminated depths (Uiblein, 1995). While this observation fits well with the assumed antipredator function of the ocellus, a posterior shift in the position of this color structure found in the Gulf of Aden population required alternative interpretations. In a subsequent study of coloration patterns 50 Neobythites species, 22 species were found to have well-developed ocelli (Uiblein and Nielsen, 2005, Fig. 1). Among co-occurring species considerable variation in ocellus position and number occurred which suggests a social communication function that would limit interspecific interactions and hybridization (Uiblein and Nielsen, 2005). Thus, ocelli in Neobythites may serve two different functions, minimization of predation risk and social communication for enhancement of species recognition. Direct evidence from in-situ or ex-situ behavioral observations
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